Table 2 Studies reporting bacterial co-infection in patients with COVID-19

Alharty et al., 2020 (1)

Critically ill

Nosocomial acquired bacterial infection by culture (15 VAP + 10 CLI)

Most common: Acinetobacter baumannii, and MRSA

Allou et al., 202 1(2)

Not specific: General including critically ill

Co-infections. Method: Measured by multiplex PCR, pneumococcal and Legionella urinary antigen tests, cytobacteriological examination of sputum cultures, and serology of atypical respiratory pathogens

Branhamella catarrhalis = 1

Streptococcus pneumoniae and Haemophilus influenza = 1

MSSA = 1

Amit et al., 2020 (3)

Critically ill

Secondary infection. Method: NR

NR

Asmarawati et al., 2021 (4)

Moderate to Critically ill

Expressed as co-infection and secondary infections

Method: Blood and sputum and urine cultures

Most common presented

Blood culture: ESBL-producing Klebsiella pneumoniae, Pseudomonas spp.

Sputum: Acinetobacter baumannii, Klebsiella pneumoniae

Ayding Bahat et al., 2020 (5)

Haemodialysis

Secondary infection. Method: NR

NR

Balena et al., 2020 (6)

Elderly

At least one secondary infection by authors. Method: NR

NR

Baraboutis et al., 2020 (7)

Overall

Blood and sputum cultures, urine pneumococcal and legionella antigen

NR

Bardi et al., 2021 (8)

Not specific: General

Nosocomial infection (30 LRTI, 21 VAP, 28 BSI, 24 CRBSI, 7 UTI, 2 soft tissue infections)

Method: Cultures

Most common presented:

BSI: Enterococcus faecium (43%), followed by Enterococcus faecalis (21%)

CRBSI: coagulase-negative staphylococci (54%), Enterococus faecium (17%)

VAP: Staphylococcus aureus (24%)

Barrasa et al., 2020 (9)

Critically ill

NR

NR

Barry et al., 2020 (10)

Not specific: General including critically ill

Method: Sputum culture and blood culture

Sputum culture: Stenotrophomonas maltophilia = 1, Klebsiella pneumoniae = 1

Blood culture: Staphylococcus epidermidis = 4; Enterococcus faecalis = 1; Corynebacterium amycolatum = 1; Bacillus pumilus = 1

Basakaran et al., 2021 (11)*

Critically ill

Method: Standard culture (blood, sputum, tracheal-aspirate, bronchoalveolar lavage, urine) and validated culture-independent tests such as respiratory viral PCR and urinary antigens

The most common potential co-pathogens identified were Gram negative bacteria, including Klebsiella spp. (23) and Escherichia coli (20)

Bhatt et al., 2021 (12)

Not specific: General including critically ill

Method: Blood culture

Most common: Staphylococcus epidermidis, MSSA

Enterococcus faecalis, Escherichia coli, MRSA

Chen et al., 2020 (14)

Elderly

Method: PCR

Mycoplasma pneumoniae = 2

Chen et al., 2021 (15)*

Not specific: General

Method: Blood culture, respiratory culture, serology, PCR and metagenomic next-generation sequencing

Mycoplasma pneumoniae = 3

Haemophilus influenzae = 6

Klebsiella pneumoniae = 2

Streptococcus pneumoniae = 1

Staphylococcus aureus + Streptococcus pneumoniae = 1

Staphilococcus aureus + Haemophilus influenzae = 1

MRSA + Haemophilis influenzae + Streptococcus pneumoniae = 1

Cheng et al., 2020 (16)*

Not specific: General including critically ill

Method: Blood culture, respiratory culture, serology, PCR

MSSA + Haemophilus influenzae = 1, MSSA = 8, Pseudomonas aeruginosa = 1, Haemophilus influenza = 2

Chengy et al., 2020 (17)

Not specific: General

Method: Positive culture or clinical/laboratory suspicion

NR

Chong et al., 2021 (18)*

Not specific: General including critically ill

Method: Respiratory tract cultures ± concurrent positive blood culture

Haemophilus influenzae = 3, Klebsiella penumoniae = 3

Pseudomona aeruginosa + MSSA = 3, Corynebacterium striatum = 2

MRSA = 2

Others = Citrobacter freundii, Moraxella catarrhalis, Enterobacter aerogenes, Klebsiella aerogenes (respiratory culture)

Choubey et al., 2021 (19)

Not specific: General

Method: Mycoplasma pneumoniae serology

Mycoplasma pneumoniae = 8

Contou et al., 2020 (20)*

Critically ill

Method: Cultures, PCR, antigen

Most common: MSSA (10/32, 31%), Haemophilus influenzae (7/32, 22%), Streptococcus pneumoniae (6/32, 19%), Enterobacteriaceae spp. (5/32, 16%)

D’Onofrio et al., 2020 (21)*

Not specific: General including critically ill

Method: Cultures, PCR, antigen

Staphylococus hominis = 1, Corynebacterium aurimucosum = 1, Streptococcus pyogenes = 1

Desai et al., 2020 (22)

Not specific: General

Method: Streptococcus pneumoniae urinary antigen (u-Ag)

Streptococcus pneumoniae = 68

Dolci et al., 2020 (23)

Not specific: General

Definition/Method: positivity of blood cultures and/or of cultures of lower respiratory tract specimens (bronchoalveolar lavage fluid or bronchial aspirate)

NR

Ekadashi et al., 2021 (24)

Not specific: General including critically ill

Blood culture

Coagulase negative Staphylococcus spp. (11, 73.3%)

Elabbadi et al., 2021 (25)*

Critically ill

Method: Culture (respiratory, blood), urinary antigen

Gram positive = 11, Gram negative = 13

Falcone et al., 2021 (26)*

Not specific: General including critically ill

Definition: Hospital acquired > 48 h

Method: Blood culture

Enterobacterales (44.9%), non-fermenting Gram negative bacilli (15.6%), Gram positive bacteria (15.6%)**

Garcia-Vidal., 2021 (28)*

Not specific: General including critically ill

Method: Culture (respiratory, blood), urinary antigen. < 24 h

Streptococcus pneumoniae + Moraxella catarrhalis = 1

Staphylococcus aureus + Haemophilus influenzae = 1

Gayam et al., 2020 (29)*

Not specific: General

Method: Mycoplasma PCR

Mycoplasma pneumoniae = 6

Goncalves et al., 2021 (30)*

Not specific: General

Definition/Method: Clinical features and positive blood, sputum, urine, or tissue culture results

NR

Guan et al., 2020 (31)

Not specific: General

Method: Blood and respiratory culture

Gram negative bacteria = 2

Gram negative + Gram positive bacteria = 3

He et al., 2020 (32)

Not specific: General

Method: PCR

Streptococcus pneumoniae = 14, Bordetella pertussis = 19, Streptococcus.pyogenes = 3, Staphylococcus aureus = 1, Mycobacterium tuberculosis = 7, Neisseria meningitidis = 7, Haemophilus influenzae = 17, Pseudomonas aeruginosa = 57

He et al., 2021 (33)*

Not specific: General

Definition/Method: Clinical diagnosis based on clinical findings combined with laboratory and radiology findings

NR

Huang et al., 2020 (34)

Not specific: General including critically ill

Definition/Method: Positive culture of a new pathogen from a lower respiratory tract specimen

NR

Huang et al., 2020 (34)

Critically illl

Definition/Method: Positive culture of a new pathogen from a lower respiratory tract specimen

NR

Huang et al., 2021 (35)

Critically illl

Method: Culture

NB: Majority of infections were considered nosocomial

NR

Hughes et al., 2020 (36)

Not specific: General

Method: Blood culture, respiratory culture, pneumococcal antigen, Legionella antigen

CRBSI: Klebsiella pneumoniae = 1, VAP: Enterobacter cloacae = 1

CLI: Enterococcus spp. = 2, Pseudomonas aeruginosa = 1

Humières et al., 2021 (37)

Critically ill

Definition/Method: Nosocomial infections. Clinical features and positive blood, sputum, urine, or tissue culture results

NR

Karaba et al., 2021 (38)*

Not specific: General

Definition/Method: Clinical, laboratory, and radiographic criteria plus microbiologic diagnosis

Only confirmed:

Sputum culture: MSSA = 1

Karami et al., 2021 (39)*

Not specific: General

Method: Respiratory cultures, pneumococcal antigen, Legionella antigen

Most common: Staphylococcus.aureus, Escherichia coli, Stenotrophomonas maltophilia

Kimming et al., 2020 (40)

Critically ill. Soc

Definition: Including hospital acquired infections

Method: Cultures

NR

Kolenda et al., 2020 (41)

Critically ill

Method: PCR and culture

Most common: Staphylococcus.aureus,and Haemophilus influenzae

Lardaro et al., 2021 (42)*

Not specific: General including critically ill

Method: Blood cultures

NR

Li et al., 2020 (a) (44)

Not specific: General

Method: Cultures

Acinetobacter baumannii (57/159, 35.8%), Klebsiella. pneumoniae (49/159, 30.8%,), Stenotrophomonas maltophilia (10/159, 6.3%)

Mady et al., 2020 (48)

Critically ill

Definition: Including hospital acquired infections

Method: Blood and respiratory cultures

Blood culture: Staphylococcus aureus = NR, Vancomycin resistant enterococcus (sensitive to tigecycline) = NR, Acinetobacter baumannii = NR

VAP: Pseudomonas spp. = 3, Acinetobacter baumannii = 3

Mahmoudi et al., 2020 (49)

Not specific: General

Method: Endotracheal and blood cultures

Klebsiella spp. (11, 25.59%), MSSA (9, 20.93%), Escherichia.coli (7, 16.28%), MRSA (6, 13.95%), Enterobacter spp. (5, 11.63%), Streptococcus pneumoniae (1, 2.32%), Pseudomonas aeruginosa (4, 9.30%)

Mason et al., 2021 (50)

Not specific: General

Method: Sputum, blood, urine ag, Mycoplasma PCR

NR

Nassir et al., 2021 (52)

Not specific: General including critically ill

Method: Blood and respiratory cultures

NR

Nebreda et al., 2020 (53)*

Not specific: General including critically ill

Method: Blood and respiratory culture

Most common: Gram negative bacilli (59%), Escherichia.coli (47%) Enterococcus faecalis (21%), Streptococcus pneumoniae (33%) and Staphylococcus aureus (33%)

Quartuccio et al., 2020 (55)

SOCa

Method: Respiratory and blood cultures

NR

Richardson et al., 2020 (56)

Not specific: General including critically ill

Method: PCR for extensive respiratory panel including atypical bacteria

Chlamydia pneumoniae = 2

Mycoplasma pneumoniae = 1

Rippa et al., 2021 (57)

Not specific: General including critically ill

Definition: Clearly stated as secondary co-infection within > 48 h of admission

BSIs: Gram positive bacteria (76/106, 71.7%), of which 53/76, 69.7% were coagulase-negative staphylococci

BSIs: Gram negative bacteria (23/106, 21.7%), of which 7/23, 30.4% Acinetobacter baumannii, and 5/23, 21.7% were Escherichia coli

LRTIs: Gram-negative bacteria (14/26, 53.8%)

Rothe et al., 2020 (58)

Not specific: General including critically ill

Method: Blood cultures, Legionella pneumophila and Streptococcus pneumoniae urinary antigens

Only blood cultures were positive (n = 10)

Shah et al., 2020 (60)

Overall

Method: Blood and respiratory cultures

Blood culture: Enterococcus faecium = 1

Respiratory culture: Stenotrophomonas maltophilia = 1

Shao et al., 2020 (61)

Not specific: General including critically ill

NR

NR

Sharifipour et al., 2020 (62)

Critically ill

Definition: nosocomial infections

Method: Cultures

Acinetobacter baumannii (17, 90%)

Staphylococcus aureus (2, 10%)

Silva et al., 2021 (63)

Critically ill

Method: Cultures

Staphylococcus spp. (29, 45.3%), Acinetobacter spp. (21, 32.8%), Pseudomonas spp. (21, 32.8%), Stenotrophomonas spp. (9, 14.06%), Klebsiella spp. (8, 12.5%), Enterobacter spp. (6, 9.4%), Enterococcus spp. (6, 9.4%), and Escherichia coli (4, 6%)

Singh et al., 2021 (64)

Overall

Method: Cultures, serology and PCR

Heamophilus influenzae (9.27%), Staphylococcus aureus (13.17%), Streptococcus pneumoniae (1.94%)

Soogard et al., 2021 (65)*

Not specific: General including critically ill

Definition/Method: Community-acquired bacterial pneumonia was defined as a microbiology-confirmed pneumonia diagnosed concurrent with SARS-CoV-2 infection or within < 48 h of hospital admission

NR

Tang et al., 2021 (68)

Not specific: General including critically ill

Method: Mycoplasma pneumonia PCR

Mycoplasma pneumoniae = 5

Thelen et al., 2021 (69)*

Not specific: General including critically ill

Method: Blood cultures

Escherichia coli = 2, Klebsiella pneumoniae = 1, Pseudomonas aeruginosa = 1, Streptococcus pneumoniae = 2, Staphylococcus aureus = 1

Towsend et al., 2020 (70)*

Not specific: General including critically ill

Method: Cultures and urinary antigen

Pseudomonas aeruginosa, Escherichia.coli, Klebsiella pneumoniae,. Oxytoca, Klebsiella aerogenes, MSSA, Streptococcus pneumoniae

Vanhomwegen et al., 2021 (71)*

Critically ill

Method: Respiratory or blood cultures

NR

Vaughn et al., 2021 (72)*

Not specific: general

Method: Blood and sputum cultures, urine pneumococcal and legionella antigen, Mycoplasma pneumonia or Chlamydophila pneumonia PCR

NR

Wan et al., 2020 (73)

Not specific: General including critically ill

NR

NR

Wan et al., 2020 (73)

Severe and critically ill

NR

NR

Wang et al., 2020 (75)

Elderly

NR

NR

Wang et al., 2021 (76)*

Not specific: General including critically ill

Method: Blood, lower respiratory tract, urine and other cultures

Blood cultures: Escherichia coli, Klebsiella pneumoniae, Klebsiella variicola, Proteus mirabilis, MRSA, MSSA and Staphylococcus epidermidis

Respiratory cultures: Escherichia coli (ESBL-producing), group A streptococcus, Haemophilus influenzae, Pseudomonas aeruginosa, MSSA

Zhang et al., 2020 (79)

Not specific: General including critically ill

Definition/Method NR. Likely nosocomial

Mons common: A.baumannii, Escherichia coli = NR

Pseudomonas aeruginosa, Enterococcus = NR

Zhang et al., 2020 (80)

Not specific: general

Method: IgM

Mycoplasma pneumoniae = 5

Zhang et al., 2020 (81)

Critically ill

Definition: VAP

Method: Cultures

Gram negative bacteria (26, 50.00%), Gram positive bacteria (14, 26.92%), virus (6, 11.54%), fungi (4, 7.69%), and others (2, 3.85%)

Zhang et al., 2021 (83)

Elderly

NR

NR

Zhang et al., 2020 (84)

Not specific: general

NR

NR